Peter Frost's anthropology blog, with special reference to sexual selection and the evolution of skin, hair, and eye pigmentation

Monday, March 17, 2008

Testosterone and paternal investment

As modern humans moved north into environments with longer winters, women were less able to feed themselves and their children through food gathering. They thus became more dependent on food from their male partners. For men, this greatly increased the cost of having a wife and children, thus making polygyny prohibitively expensive for all but the ablest hunters.

Initially, this situation came about by men and women pushing their respective envelopes of behavioral plasticity. It may not have been the happiest of situations, but circumstances left no other choice. Over time, however, natural selection should have improved things by favoring men who were less predisposed to polygyny and more predisposed to provide for their wives and children.

How? Apparently, by lowering testosterone levels in men once they’ve entered a pair bond. This has been shown by findings recently presented at this year’s annual meeting of the American Association of Physical Anthropologists. According to Shur et al. (2008):

Numerous studies reveal a negative correlation between testosterone concentration and paternal care in diverse mammals including nonhuman primates and humans. Several researchers suggest that spousal investment accounts for the lower testosterone of married men compared to unmarried men, but findings that the lowest testosterone levels are observed in married men with children implicate paternal care as particularly relevant. Thus testosterone reduction may reflect a facultative shift in male reproductive strategy from intrasexual competition and copulation to care of young.

This hypothesis was tested with wild olive baboons, among whom lactating females form close “friendships” with their male partners.

In contrast to control males, male friends experienced a decrease in testosterone level coinciding with the birth of their female friends’ infants. Male friends also maintained a lower basal testosterone level than did control males during the lactation period of their female friends. Testosterone levels in male friends increased gradually corresponding with developing infant independence.

This finding may explain the marked differences in testosterone levels we see in humans, particularly between tropical and non-tropical populations. These levels seem to decrease wherever men compete less keenly for mates (because polygyny is less common) and wherever they invest more in parenting. Lowering the level of testosterone seems to lower the threshold for expression of paternal investment.

If the testosterone level has fallen in some populations because of selection for paternal investment, we should see evidence of such selection elsewhere, e.g., altered spatial distribution of testosterone receptors in the brain, more mental space dedicated to parenting behavior, etc.

19 comments:

"Marked" differences are seen in T levels between Western and non-Western populations, not "tropical" and non-tropical. See here and here. T levels are elevated in Westerners (Americans and Europeans) relative to almost every other population which has been studied, including those from Africa.

The black-white differences in T sometimes observed in the U.S. are not what I would call marked--and where they exist at all, they are plausibly explained in terms of environment (see Allan Mazur's "honor subcultures" hypothesis).

It's not impossible that populations vary genetically in basal T levels, but this has yet to be demonstrated (certainly not in the direction assumed by you and Rushton primarily on the basis of a single 1986 study on Los Angeles college students) and the impression I get from reading the literature is that any innate population differences are likely to be swamped by situational and environmental factors.

On the other hand, black men have consistently (from the earliest studies in the 1940s to today) been found to have higher estrogen levels than white men, both in the United States and in Africa. Not sure how this fits into your theory.

Note: I don't deny that blacks have higher rates of violent criminality, STDs, and so on. What I deny is that population differences in T are some sort of elegant explanation for these differences, as argued by Rushton.

I suspect that differences in general intelligence alone can explain most of the black-white gap in criminality and promiscuity. If after controlling for IQ significant differences remain, my guess is they are more likely to be explained by differences in e.g. MAOA rather than T.

Hispanics (primarily Amerindian-Caucasoid mixes) have rates of criminality and STDs intermediate between those of blacks and whites. Their IQs also just happen to be intermediate. But going by Rushton we would expect them to have innately lower T than whites and therefore lower criminality.

(In reality, at least one study found Hispanic men in America to have higher circulating T than both black and white men; I suspect "honor subcultures" are again implicated. This is not, however, a point in favor of "T causes crime" since we would then expect Hispanics rather than blacks to be the most criminal. Plus, I believe that in South America, Hispanics combine low T and high criminality.)

When Ross et al. (1986) tested young male students, they found that mean testosterone levels were 19% higher in blacks than in whites and free testosterone levels 21% higher. When they extended their research to young Japanese subjects, they found intermediate testosterone levels but less 5α-reductase—an enzyme that converts testosterone into the physiologically more active DHT (Ross et al., 1992). Pettaway (1999) has summarized research in this area; in general, higher testosterone levels in young black men appear to be a robust, replicable finding. The race difference disappears, however, in middle-aged subjects. This may be an aging effect, as well as a paternal investment effect (middle-aged males are more likely to be married and with children).

Lifetime exposure to testosterone/DHT is also reflected in the incidence of prostate cancer, with the highest incidences being among African American men (Brawley and Kramer, 1996). Other populations of black African descent (i.e., West Indians and sub-Saharan Africans) exhibit lower incidences, but these have been shown to reflect underreporting and are probably just as high (Glover et al., 1998; Ogunbiyi and Shittu, 1999; Osegbe, 1997).

In the studies you cite from Africa, several are from hunter-gatherer populations (e.g., !Kung San, Ituri pygmies) who have very low incidences of polygyny and equally low male-male competition for mates. This point is important because the hypothesis is that high testosterone levels are an adaptive response to high male-male competition and low paternal investment.

The other studies are composed mainly of married, middle-aged or even old subjects among whom testosterone levels have fallen to the human mean. Finally, you state that Christiansen (1991) found significantly lower testosterone levels in both !Kung and ‘Namibians’ than in Western subjects. Actually, Christiansen studied !Kung San and Kavango Bantu (both of whom are Namibians). The weakly polygynous !Kung had low testosterone levels and the highly polygynous Kavango had high testosterone levels. “The Kavanago surpass the San men in all absolute mean androgen levels” (Winkler and Christiansen, 1993). Again, this finding is in line with the hypothesis.

You also cite studies on Amerindian populations (the Ache of Paraguay and the Aymara of Bolivia). These populations, as do all Amerindian populations, have low incidences of polygyny and high paternal investment.

I agree with the observation that malnutrition tends to suppress hormonal levels. This is most evident in the Harare (Zimbabwe) study, although even under ideal conditions I would not expect to see high testosterone levels in married middle-aged men.

Adjustment by analysis of covariance for time of sampling, age, weight, alcohol use, cigarette smoking, and use of prescription drugs somewhat reduced the differences. After these adjustments were made, blacks had a 15% higher testosterone level and a 13% higher free testosterone level.

Rushton and Frost choose to continually cite the pre-adjustment numbers (19%/21%) from this study. Nor can they seem to dig up any other study which comes close to replicating a difference of comparable magnitude in the desired direction.

I don't find the prostate cancer data adds to your case. Even if prostate cancer risk is directly correlated with "lifetime exposure to testosterone/DHT" within populations (and the evidence for that seems equivocal), we can not infer between population differences in T/DHT from population differences in prostate cancer.

(The opposite argument--that black men are observed to have higher androgen levels and this may help explain their higher incidence of prostate cancer--is the one actually made by researchers. It is a reasonable argument to the extent the higher androgen exposure part is true; we can't, however, flip the argument around and use it to bolster the inconsistent evidence for higher androgen levels in blacks.)

For example, genetic variants which influence susceptibility to prostate cancer may be distributed unevenly among populations (this study on Swedes suggests it's more than a possibility).

"You also cite studies on Amerindian populations (the Ache of Paraguay and the Aymara of Bolivia). These populations, as do all Amerindian populations, have low incidences of polygyny and high paternal investment."

So how do you explain the fact that--in the US, according to one recent study--Hispanics have higher circulating Testosterone levels than blacks?

Western-nonwestern differences are most pronounced among young men.

Among Americans, I'm fairly certain that at all ages white men are more likely to be married or in "committed relationships" than black men, meaning basal testosterone levels among black men will tend to be overestimated relative to whites.

I didn't state that. The Yale anthropology professor and reproductive ecology/endocrinology expert whose book chapter I excerpted wrote that. You should probably read the entire chapter (and plenty else) if you're going to play at this sort of thing.

The bottom line is that many African populations, including negroid agriculturists, have demonstrably much lower salivary testosterone than Westerners.

In the Ross et al. study the age difference between black and white subjects was only 8 months, not enough to have any bearing on testosterone levels. Heights were also similar. So the adjustment was in function of lifestyle variables (alcohol use, cigarette consumption. etc.). Such an 'adjustment' is not justified because it biases the black sample towards low-testosterone individuals.

"Nor can they seem to dig up any other study which comes close to replicating a difference of comparable magnitude in the desired direction."

Why not read the literature review I cited in my previous response? Here's the abstract:

Racial differences in the androgen/androgen receptor pathway in prostate cancer.

Pettaway CA, J Natl Med Assoc, 91(12):653-60 1999 Dec

Pathologic and epidemiologic data suggest that while little racial variation exists in prostate cancer prevalence ("autopsy cancer"), striking racial variation exists for the clinically diagnosed form of the disease. A review of the available literature was performed to define whether racial differences in serum androgen levels or qualitative or quantitative differences in the androgen receptor were correlated with prostate cancer incidence or severity.

Black men were found to be exposed to higher circulating testosterone levels from birth to about age 35 years.

Such differences were not consistently noted among older men. Significant differences also were found for dihydrotestosterone metabolites among black, white, and Asian men. Unique racial genetic polymorphisms were noted for the gene for 5 alpha-reductasetype 2 among black and Asian men. Novel androgen receptor mutations recently have been described among Japanese, but not white, men with latent prostate cancer. Finally, androgen receptor gene polymorphisms leading to shorter orlonger glutamine and glycine residues in the receptor protein are correlated with racial variation in the incidence and severity of prostate cancer. This same polymorphism also could explain racial variation in serum prostate-specific antigen levels.

Collectively, these data strongly suggest racial differences within the androgen/androgen receptor pathway not only exist but could be one cause of clinically observed differences in the biology of prostate cancer amongracial groups.

"So how do you explain the fact that--in the US, according to one recent study--Hispanics have higher circulating Testosterone levels than blacks?"

Reference, please.

"Among Americans, I'm fairly certain that at all ages white men are more likely to be married or in "committed relationships" than black men, meaning basal testosterone levels among black men will tend to be overestimated relative to whites."

The race difference disappears by middle age. This is partly because middle-aged men are more likely to be married and parenting. The main reason, however, is an age effect. Testosterone levels decline with age, and the decline is more marked in groups that start off with high testosterone levels.

"The bottom line is that many African populations, including negroid agriculturists, have demonstrably much lower salivary testosterone than Westerners."

I fully agree with you if you're talking about weakly polygynous hunter-gatherers. If you're talking about highly polygynous agriculturalists, I strongly disagree. The studies you cite are based largely on middle-aged or even elderly subjects.

"I didn't state that. The Yale anthropology professor and reproductive ecology/endocrinology expert whose book chapter I excerpted wrote that."

If you quote someone to back your argument, you assume responsibility for the quote's truthfulness. That's the way things work.

So the adjustment was in function of lifestyle variables (alcohol use, cigarette consumption. etc.). Such an 'adjustment' is not justified because it biases the black sample towards low-testosterone individuals.

You make no sense. It's entirely appropriate to control for confounds like smoking:

Smoking men had significantly higher levels of total and free testosterone compared with men who never smoked (p < 0.001 and <0.01 respectively). Both total and free testosterone levels increased significantly with increasing number of cigarettes smoked daily (p < 0.001). Smoking men had 15% higher total and 13% higher free testosterone levels compared with men who never smoked. Thus, smoking seems to be an important confounding factor when evaluating testosterone levels, and could possibly mask borderline hypogonadism.

Apart from the fact that it's published in an irrelevant journal and would be inconvenient to obtain? (Have you read it?) I don't need to read it to know that it cites the 1986 Ross article and little or nothing else which supports substantial black-white differences in circulating T. If it were otherwise, you, Rushton, and dozens of prostate cancer researchers would not need to lean so heavily on a single study to establish that supposed fact.

"So how do you explain the fact that--in the US, according to one recent study--Hispanics have higher circulating Testosterone levels than blacks?"

I fully agree with you if you're talking about weakly polygynous hunter-gatherers. If you're talking about highly polygynous agriculturalists, I strongly disagree. The studies you cite are based largely on middle-aged or even elderly subjects.

"You make no sense. It's entirely appropriate to control for confounds like smoking"

Smoking and drinking are both seen as indicating adherence to male values. These social indicators thereby provide a means to elevate one's status within the male hierarchy and improve sexual access to women. This is as true in the U.S. as it is in Europe (where the Svartberg study was conducted). Young men who don't drink or smoke thus represent a subpopulation with generally lower testosterone levels.

"Apart from the fact that it's published in an irrelevant journal and would be inconvenient to obtain? (Have you read it?) I don't need to read it"

Sigh. No comment.

"Young (15 to <30) Americans have markedly higher salivary T than Congolese (specifically, Lese farmers--these are not pygmies or hunter-gatherers) in the same age bracket."

1. The young Americans in that study are simply identified as .... young Americans. That demographic is now less than 60% of European descent for the U.S. as a whole. If we look at where the study was conducted (Massachusetts, essentially Boston), we find that, in 2005, Boston public schools were 46% black and 31% Latino (mainly of Puerto Rican and Dominican descent). The study population was thus largely of African or part-African descent.

2. The Lese population has long been receiving gene flow from Pygmy hunter-gatherers. At present, about 13% of Efe (pygmy) women are married to Lese villagers. To a large degree, it reflects selection pressures that have acted on a weakly polygynous population.

Again, I agree with the point you made earlier that malnutrition or undernutrition probably depresses testosterone levels in Africa.

"http://jcem.endojournals.org/cgi/rapidpdf/jc.2007-0028v1.pdf"

In the short version of the article, the subjects are identified as "A total of 1413 men aged 20+ yr". Considering that t levels decline markedly even between 24 and 30 years of age, such a lack of control for age could easily produce spurious ethnic differences and obscure real ones. I'll consult the long version at the university library, but I doubt that it will be more informative.

Young men who don't drink or smoke thus represent a subpopulation with generally lower testosterone levels.

Citation? Or are you just pulling this out of your ass? All the research I've seen suggests smoking elevates testosterone. I believe drinking depresses testosterone (and white men tend to be heavier drinkers), though I don't have time to check that right now.

You have no basis on which to assume the young American sample reflects the racial makeup of the Boston public school system. At least one study by the same group mentions using a sample of Harvard students. And Poles apparently have similar testosterone levels to the American sample.

As for the "Serum estrogen, but not testosterone" study, what part of "adjusting for age" don't you understand?

I don't recall writing anything like that. In fact, I recall quoting Bribiescas as follows:

. . . population variation in testosterone levels reflects hormonal release in American populations rather than hormonal suppression among nonwestern populations.

Am I missing something, or do you believe ancient Bantus had convenience stores?

The important point, however, is that environment can play a major role in determining testosterone levels and population differences reflect factors other than ancient evolutionary history.

And this is true not just when you want an excuse for low T in African farmers. Perhaps hunter-gatherers in Africa have innately lower testosterone than their "highly polygynous" neighbors, but unless you've controlled very tightly for environmental factors, you have no way to know that.

"You have no basis on which to assume the young American sample reflects the racial makeup of the Boston public school system."

Sigh. The subjects "were recruited by public advertisement." So they probably reflected the general youth demographic. In any case, without any indication of racial composition, the results are unusable.

"As for the "Serum estrogen, but not testosterone" study, what part of "adjusting for age" don't you understand?"

I have now read the full text. According to the authors, the study population was one "in which Mexican-Americans,non-Hispanic blacks, and the elderly wereover-sampled." In other words, a disproportionate number of subjects were elderly. Remember, the black-white difference in testosterone levels begins to shrink after 24 and is gone by 35.

The Hispanic population is also younger than other groups, including African Americans. So if age is not controlled, t levels will inevitably be higher on average among Hispanic subjects.

Rohrmann et al. broke their data down into three age classes: 20-44; 45-69; and 70+. Unfortunately, testosterone levels decline markedly in black men from 24 years of age onward. By 35, the black-white difference is gone.

The first age class (20-44)is simply too broad to capture the black-white difference. The median ages were 31.8 for whites, 29.5 for blacks, and 28.6 for hispanics. This difference in median age probably accounts for the higher t levels of the hispanic subjects.

"And you realize, I hope, that the entire point of oversampling is to be able to make statistically sound analyses of subsamples?"

Yes, but the point at issue here is not t levels in older men; it's t levels in very young men, essentially the 15 to 25 demographic.

I know we're on the Internet and all, but this belligerent chest-beating is unnecessary. Anonymity does not justify incivility, and you should be banned if you can't have an argument over facts without being an unpleasant troll about it.

The new study cited (2007) is the best evidence that testosterone does not differ between whites and blacks, but even the authors admit the three previous studies that checked found this difference among younger blacks and whites. This is the Ross study, but also the Ellis study and the Winters study from 2001.

Furthermore, we know blacks have more androgen receptors than whites and Asians - so all else is not equal. Blacks with the same amount of T, are still processing more hormone.

Furthermore, we know from digit ratios that black populations (in Africa, America, and the Caribbean) all get a higher dose of prenatal (or developmental) testosterone than all 25+ European populations examined thus far (with the possible exception of Finns). Prenatal testosterone exposure is linked to masculine development, athletic ability, creativity, and sexual behavior.

I suspect that differences in general intelligence alone can explain most of the black-white gap in criminality and promiscuity.

Herrnstein and Murray controlled for IQ and found it accounted for most of the income and occupational differences, but far less of the behaviors related to criminality and reproduction (which are closely related domains). Only 8% of the B-W marriage gap was accounted for by IQ. Also, controlling for IQ, blacks are still 2 and half times more likely to be incarcerated than whites (as opposed to six to seven times without the control).

That's some pretty sad tap dancing, Peter. Maybe try (1) thinking your criticisms all the way through, and (2) turning that same critical eye to studies that tell you what you want to hear.

Assuming the following is true:- "By 35, the black-white difference is gone."- "The median ages were 31.8 for whites, 29.5 for blacks, and 28.6 for hispanics."

This claim is a bizarre non sequitur:

"The first age class (20-44)is simply too broad to capture the black-white difference."

Assuming older (35+) black and white men have identical testosterone levels (which is not what Rohrmann finds--the black-white difference is larger for 45-69 year olds), in a sample with a median age below 30 the signal from the supposed markedly elevated T in young blacks ought to be clear.

Moreover, I find it hilarious you claim an 11 month age difference "probably accounts for the higher t levels of the hispanic subjects". Earlier, where black-white differences are concerned, 8 months is "not enough to have any bearing on testosterone levels." Meanwhile, the 2.3 year age black-white age difference in Rohrmann doesn't concern you either.

Did I miss where Peter Frost appointed prissy foreigner "rain and" to moderate his comments section?

Furthermore, we know blacks have more androgen receptors than whites and Asians - so all else is not equal. Blacks with the same amount of T, are still processing more hormone.

We don't know that all else is equal.

Furthermore, we know from digit ratios that black populations (in Africa, America, and the Caribbean) all get a higher dose of prenatal (or developmental) testosterone than all 25+ European populations examined thus far (with the possible exception of Finns).

Considering the gross differences in skeletal morphology between blacks and whites (greater bone density and distally-elongated limbs in blacks), there's no a priori reason to believe that just because digit ratio within a population weakly tracks prenatal androgen exposure, the same is true when comparing blacks and whites.

Even if greater prenatal testosterone in blacks is demonstrated (and it wouldn't surprise me, at least in the U.S. case--black women are fatter/heavier, which would tend to jack up their testosterone levels even if black and white women have genetically identical T levels), again there's little basis for generalizing any particular interpopulation differences from the intrapopulation correlations. Or do you believe blacks are more "creative"?

Also, controlling for IQ, blacks are still 2 and half times more likely to be incarcerated than whites (as opposed to six to seven times without the control).

In other words, you're saying "differences in general intelligence alone can explain most of the black-white gap in criminality"?

Only 8% of the B-W marriage gap was accounted for by IQ.

Oh, I don't doubt physical and personality differences play a role in that disparity. Just not in the direction Steve Sailer and other negroid jock sniffers would like to believe.

My last reply assumed you were talking about black-white intermarriage rates.

If you are talking about just plain marriage rates, I'm still not too surprised. Considering the spike in illegitimacy for all groups over the past half century, obviously factors other than just biology are at play. (And among potential biological factors, I've certainly never seen it demonstrated that testosterone plays a major role in race differences in e.g. illegitimacy rates.)

"Assuming older (35+) black and white men have identical testosterone levels (which is not what Rohrmann finds--the black-white difference is larger for 45-69 year olds), in a sample with a median age below 30 the signal from the supposed markedly elevated T in young blacks ought to be clear."

First, the black-white difference reverses after the early thirties (see references in my next post), so the signal from blacks below 24 years of age would be washed out.

Yes, Rohrmann et al. found higher t levels in black men than in white men in the 45-69 age group. But t levels decline from 45 to 69 in both blacks and whites, and we know nothing about how the age distribution of these subjects within the 45-69 age group. Unlike other studies, Rohrmann et al. only provide median age and not mean age, although the latter measure would have been more informative about the relative youthfulness of these subsamples.

It is curious, to put it mildly, that the 45-69 year old black men had higher t levels (5.62) than the 20-44 year old black men (5.35). This is contrary to the literature on variation in t levels with age and suggests there may have been some data tampering.

"Moreover, I find it hilarious you claim an 11 month age difference "probably accounts for the higher t levels of the hispanic subjects". Earlier, where black-white differences are concerned, 8 months is "not enough to have any bearing on testosterone levels." Meanwhile, the 2.3 year age black-white age difference in Rohrmann doesn't concern you either."

The answer is simple: t levels don't start to decline until about 24 years of age. The need to control the results for age becomes unavoidable after 24. Moreover, the age differences in the Rohrmann et al. study are given only in median ages, not in mean ages. The age disparity would have been greater if mean ages had been used.

On a final note, I realize you feel strongly about this subject. It is possible, however, to make one's views known without resorting to insults and invective.

Welcome to my blog! For the most part, this page will be an extension of my website, with comments relating to my research. But it will also branch out into more general discussions of human evolution.